Harvest Event is haunted by the ghost of Zepheniah Mann, who is larger than the ghosts in Eyeaduct and topped with his personal Ghastly Gibus. He appears at certain spots in the map before following a predetermined route, shortly after which he will disappear. During his brief appearances, the nearby lights will dim and he will echo moans. If any player strays too close, Zepheniah's ghost will utter a boo and scare the player, haunting them for several seconds. Between his hauntings, the Harvest Event ghost is kept floating in a tiny secret room underneath the control point.

The ghosts on Eyeaduct behave similarly to Zepheniah's ghost, but do not dim the lights, and only spawn after a team captures the control point. Multiple ghosts can be active in Eyeaduct at the same time and will disappear after scaring a player.

Ghosts spawn on Ghost Fort, but only after the control point is captured and the Wheel of Fate determines it. Seven ghosts can also be found lurking in the bottomless pit, one of which is wearing a Ghastly Gibus, much like Zepheniah Mann's ghost.

The ghost of Zepheniah can also be seen watching over the battle at the tower in Helltower, observing as the corpses of his murdered sons Redmond and Blutarch are escorted into Hell by the mercenaries. The ghost will briefly vanish from the tower during The Witching Hour before reappearing once the ghostly bridge disappears. Any player stuck on the tower after the witching hour will be stunned by Zephaniah for an infinite amount of time, at least until the witching hour begins.

In Hell, players turn into ghosts upon dying, whether by environmental death or by being killed by another player. They are given an infinite jump to let them "fly" around; and primary fire will make the ghost say "Boo!", although it will not scare players as the ghosts on Harvest will; otherwise, players are unable to attack or interact with other players. Ghost players are also unable to pick up the book inside Skull Island and thus cannot complete the Hat Out Of HellBereavement.

Killing a player while they are scared by the ghost during the annual Halloween Special will grant the player the Scared StiffScarechievement. Additionally, a player scared by the ghost will count towards certain stun related achievements.